Age-Dependent Impairment of Eyeblink Conditioning in Prion Protein-Deficient Mice

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Kishimoto, Yasushi ^a,g   Hirono, Moritoshi ^b,h   Atarashi, Ryuichiro ^c   Sakaguchi, Suehiro ^d   Yoshioka, Tohru ^e   Katamine, Shigeru ^c,f   Kirino, Yutaka ^a,g  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^d UNIVERSITY OF TOKUSHIMA   (Japan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^f NAGASAKI UNIVERSITY   (Japan)

^g TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^h DOSHISHA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; PRION PROTEIN; PRION PROTEIN LIKE PROTEIN; UNCLASSIFIED DRUG;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CEREBELLUM CORTEX; CEREBELLUM DEGENERATION; CONDITIONED REFLEX; CONDITIONING; CONTROLLED STUDY; EYEBLINK CONDITIONING; EYELID REFLEX; LEARNING; MOTOR CONTROL; MOTOR LEARNING; MOUSE; NONHUMAN; PROTEIN FUNCTION; RESPONSE TIME; STRAIN DIFFERENCE; TASK PERFORMANCE;

AGING; ANIMALS; BASE SEQUENCE; BLINKING; CONDITIONING, OPERANT; DNA PRIMERS; MICE; POLYMERASE CHAIN REACTION; PRIONS;

ANIMALIA; MUS;

EID: 84876026829     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060627     Document Type: Article

References (96)

1. Collinge J, (1999) Variant Creutzfeldt-Jakob disease. Lancet 354: 317-323.
2. Gajdusek DC, (1977) Unconventional viruses and the origin and disappearance of kuru. Science 197: 943-960.
3. Horwich AL, Weissman JS, (1997) Deadly conformations-protein misfolding in prion disease. Cell 89: 499-510.
4. Prusiner SB, (1997) Prion diseases and the BSE crisis. Science 278: 245-251.
5. Prusiner SB, (1998) Prions. Proc Natl Acad Sci USA 95: 13363-13383.
6. Masullo C, Salvatore M, Macchi G, Genuardi M, Pocchiari M, (1994) Progressive dementia in a young patient with a homozygous deletion of the PrP gene. Ann N Y Acad Sci 724: 358-360.
7. Schulz-Schaeffer WJ, Giese A, Windl O, Kretzschmar HA, (1996) Polymorphism at codon 129 of the prion protein gene determines cerebellar pathology in Creutzfeldt-Jakob disease. Clin Neuropathol 15: 353-357.
8. Bueler H, Fischer M, Lang Y, Bluethmann H, Lipp HP, et al. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356: 577-582.
9. Kuwahara C, Takeuchi AM, Nishimura T, Haraguchi K, Kubosaki A, et al. (1999) Prions prevent neuronal cell-line death. Nature 400: 225-226.
10. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I, et al. (1994) 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 8: 121-127.
11. Moore RC, Lee IY, Silverman GL, Harrison PM, Strome R, et al. (1999) Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J Mol Biol 292: 797-817.
12. Sakaguchi S, Katamine S, Shigematsu K, Nakatani A, Moriuchi R, et al. (1995) Accumulation of proteinase K-resistant prion protein (PrP) is restricted by the expression level of normal PrP in mice inoculated with a mouse-adapted strain of the Creutzfeldt-Jakob disease agent. J Virol 69: 7586-7592.
13. Sakaguchi S, Katamine S, Nishida N, Moriuchi R, Shigematsu K, et al. (1996) Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380: 528-531.
14. Nishida N, Katamine S, Shigematsu K, Nakatani A, Sakamoto N, et al. (1997) Prion protein is necessary for latent learning and long-term memory retention. Cell Mol Neurobiol 17: 537-545.
15. Nishida N, Tremblay P, Sugimoto T, Shigematsu K, Shirabe S, et al. (1999) A mouse prion protein transgene rescues mice deficient for the prion protein gene from purkinje cell degeneration and demyelination. Lab Invest 79: 689-697.
16. Li A, Sakaguchi S, Atarashi R, Roy BC, Nakaoke R, et al. (2000) Identification of a novel gene encoding a PrP-like protein expressed as chimeric transcripts fused to PrP exon 1/2 in ataxic mouse line with a disrupted PrP gene. Cell Mol Neurobiol 20: 553-567.
17. Westaway D, Daude N, Wohlgemuth S, Harrison P, (2011) The PrP-like proteins Shadoo and Doppel. Top Curr Chem 305: 225-256.
18. Moore RC, Mastrangelo P, Bouzamondo E, Heinrich C, Legname G, et al. (2001) Doppel-induced cerebellar degeneration in transgenic mice. Proc Natl Acad Sci USA 98: 15288-15293.
19. Li A, Sakaguchi S, Shigematsu K, Atarashi R, Roy BC, et al. (2000) Physiological expression of the gene for PrP-like protein, PrPLP/Dpl, by brain endothelial cells and its ectopic expression in neurons of PrP-deficient mice ataxic due to Purkinje cell degeneration. Am J Pathol 157: 1447-1452.
20. Mo H, Moore RC, Cohen FE, Westaway D, Prusiner SB, et al. (2001) Two different neurodegenerative diseases caused by proteins with similar structures. Proc Natl Acad Sci USA 98: 2352-2357.
21. Behrens A, Genoud N, Naumann H, Rulicke T, Janett F, et al. (2002) Absence of the prion protein homologue Doppel causes male sterility. EMBO J 21: 3652-3658.
22. Legname G, Nelken P, Guan Z, Kanyo ZF, DeArmond SJ, et al. (2002) Prion and doppel proteins bind to granule cells of the cerebellum. Proc Natl Acad Sci USA 99: 16285-16290.
23. Peoc'h K, Serres C, Frobert Y, Martin C, Lehmann S, et al. (2002) The human "prion-like" protein Doppel is expressed in both Sertoli cells and spermatozoa. J Biol Chem 277: 43071-43078.
24. Sakurai-Yamashita Y, Sakaguchi S, Yoshikawa D, Okimura N, Masuda Y, et al. (2005) Female-specific neuroprotection against transient brain ischemia observed in mice devoid of prion protein is abolished by ectopic expression of prion protein-like protein. Neuroscience 136: 281-287.
25. Silverman GL, Qin K, Moore RC, Yang Y, Mastrangelo P, et al. (2000) Doppel is an N-glycosylated, glycosylphosphatidylinositol-anchored protein. Expression in testis and ectopic production in the brains of Prnp0/0 mice predisposed to Purkinje cell loss. J Biol Chem 275: 26834-26841.
26. Yoshikawa D, Kopacek J, Yamaguchi N, Ishibashi D, Yamanaka H, et al. (2007) Newly established in vitro system with fluorescent proteins shows that abnormal expression of downstream prion protein-like protein in mice is probably due to functional disconnection between splicing and 3′ formation of prion protein pre-mRNA. Gene 386: 139-146.
27. Kopacek J, Sakaguchi S, Shigematsu K, Nishida N, Atarashi R, et al. (2000) Upregulation of the genes encoding lysosomal hydrolases, a perforin-like protein, and peroxidases in the brains of mice affected with an experimental prion disease. J Virol 74: 411-417.
28. Shmerling D, Hegyi I, Fischer M, Blattler T, Brandner S, et al. (1998) Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93: 203-214.
29. Weissmann C, Aguzzi A, (1999) Perspectives: neurobiology. PrP's double causes trouble. Science 286: 914-915.
30. Kim JJ, Thompson RF, (1997) Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends Neurosci 20: 177-181.
31. Thompson RF, Kim JJ, (1996) Memory systems in the brain and localization of a memory. Proc Natl Acad Sci USA 93: 13438-13444.
32. Thompson RF, Krupa DJ, (1994) Organization of memory traces in the mammalian brain. Annu Rev Neurosci 17: 519-549.
33. Attwell PJ, Cooke SF, Yeo CH, (2002) Cerebellar function in consolidation of a motor memory. Neuron 34: 1011-1020.
34. Bracha V, (2004) Role of the cerebellum in eyeblink conditioning. Prog Brain Res 143: 331-339.
35. Krupa DJ, Thompson JK, Thompson RF, (1993) Localization of a memory trace in the mammalian brain. Science 1260: 989-991.
36. Mauk MD, (1997) Roles of cerebellar cortex and nuclei in motor learning: contradictions or clues? Neuron 18: 343-346.
37. Raymond JL, Lisberger SG, Mauk MD, (1996) The cerebellum: a neuronal learning machine? Science 272: 1126-1131.
38. Yeo CH, Hesslow G, (1998) Cerebellum and conditioned reflexes. Trends Cogn Sci 2: 322-330.
39. Jiménez-Díaz L, Navarro-López J de D, Gruart A, Delgado-García JM, (2004) Role of cerebellar interpositus nucleus in the genesis and control of reflex and conditioned eyelid responses. J Neurosci 24: 9138-9145.
40. McCormick DA, Thompson RF, (1984) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223: 296-299.
41. Porras-García E, (2010) Sánchez-Campusano R, Martinez-Vargas D, Domínguez-del-Toro E, Cendelín J, et al (2010) Behavioral characteristics, associative learning capabilities, and dynamic association mapping in an animal model of cerebellar degeneration. J Neurophysiol 104: 346-365.
42. Sánchez-Campusano R, Gruart A, Delgado-García JM (2007) The cerebellar interpositus nucleus and the dynamic control of learned motor responses. J Neurosci 27: 6620-6632.
43. Sánchez-Campusano R, Gruart A, Delgado-García JM (2009) Dynamic associations in the cerebellar-motoneuron network during motor learning. J Neurosci 29: 10750-10763.
44. Welsh JP, Harvey JA, (1989) Cerebellar lesions and the nictitating membrane reflex: performance deficits of the conditioned and unconditioned response. J Neurosci 9: 299-311.
45. Yeo CH, Hardiman MJ, Glickstein M, (1985) Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60: 99-113.
46. Laine J, Marc ME, Sy MS, Axelrad H, (2001) Cellular and subcellular morphological localization of normal prion protein in rodent cerebellum. Eur J Neurosci 14: 47-56.
47. Salès N, Rodolfo K, Hassig R, Faucheux B, Di Giamberardino L, et al. (1998) Cellular prion protein localization in rodent and primate brain. Eur J Neurosci 10: 2464-2471.
48. Tanji K, Saeki K, Matsumoto Y, Takeda M, Hirasawa K, et al. (1995) Analysis of PrPc mRNA by in situ hybridization in brain, placenta, uterus and testis of rats. Intervirology 38: 309-315.
49. Buonomano DV, Mauk MD, (1994) Neural network model of the cerebellum: Temporal discrimination and the timing of motor responses. Neural Comp 6: 38-55.
50. Garcia KS, Mauk MD, (1998) Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37: 471-480.
51. Gerwig M, Hajjar K, Dimitrova A, Maschke M, Kolb FP, et al. (2005) Timing of conditioned eyeblink responses is impaired in cerebellar patients. J Neurosci 25: 3919-3931.
52. Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD, (2000) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20: 5516-5525.
53. Perrett SP, Ruiz BP, Mauk MD, (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13: 1708-1718.
54. Kishimoto Y, Kano M, (2006) Endogenous cannabinoid signaling through the CB1 receptor is essential for cerebellum-dependent discrete motor learning. J Neurosci 26: 8829-8837.
55. Kishimoto Y, Fujimichi R, Araishi K, Kawahara S, Kano M, et al. (2002) mGluR1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Eur J Neurosci 16: 2416-2424.
56. Kishimoto Y, Oku I, Nishigawa A, Nishimoto A, Kirino Y, (2012) Impaired long-trace eyeblink conditioning in a Tg2576 mouse model of Alzheimer's disease. Neurosci Lett 506: 155-159.
57. Kishimoto Y, Kirino Y (2013) Presenilin 2 mutation accelerates the onset of impairment in trace eyeblink conditioning in a mouse model of Alzheimer's disease overexpressing human mutant amyloid precursor protein. Neurosci Lett In press. doi: 10.1016/j.neulet.2013.01.025.
58. Kishimoto Y, Suzuki M, Kawahara S, Kirino Y, (2001) Age-dependent impairment of delay and trace eyeblink conditioning in mice. Neuroreport 12: 3349-3352.
59. Weissmann C, Bueler H, Fischer M, Sailer A, Aguzzi A, et al. (1994) PrP-deficient mice are resistant to scrapie. Ann N Y Acad Sci 724: 235-240.
60. Bao S, Chen L, Thompson RF, (1998) Classical eyeblink conditioning in two strains of mice: conditioned responses, sensitization, and spontaneous eyeblinks. Behav Neurosci 112: 714-718.
61. Gruart A, López-Ramos JC, Muñoz MD, Delgado-García JM, (2008) Aged wild-type and APP, PS1, and APP+PS1 mice present similar deficits in associative learning and synaptic plasticity independent of amyloid load. Neurobiol Dis 30: 439-450.
62. Woodruff-Pak DS, Logan CG, Thompson RF (1990) Neurobiological substrates of classical conditioning across the life span. Ann N Y Acad Sci 608: 150-173; discussion 74-78.
63. Woodruff-Pak DS, Papka M, Romano S, Li YT, (1996) Eyeblink classical conditioning in Alzheimer's disease and cerebrovascular dementia. Neurobiol Aging 17: 505-512.
64. López-Ramos JC, Jurado-Parras MT, Sanfeliu C, Acuña-Castroviejo D, Delgado-García JM, (2012) Learning capabilities and CA1-prefrontal synaptic plasticity in a mice model of accelerated senescence. Neurobiol Aging 33: 627.e13-26.
65. Woodruff-Pak DS, Jaeger ME, (1998) Predictors of eyeblink classical conditioning over the adult age span. Psychol Aging 13: 193-205.
66. Atarashi R, Nishida N, Shigematsu K, Goto S, Kondo T, et al. (2003) Deletion of N-terminal residues 23-88 from prion protein (PrP) abrogates the potential to rescue PrP-deficient mice from PrP-like protein/doppel-induced neurodegeneration. J Biol Chem 278: 28944-28949.
67. Tuzi NL, Gall E, Melton D, Manson JC, (2002) Expression of doppel in the CNS of mice does not modulate transmissible spongiform encephalopathy disease. J Gen Virol 83: 705-711.
68. Chen L, Bao S, Lockard JM, Kim JK, Thompson RF, (1996) Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J Neurosci 16: 2829-2838.
69. Landis SC, Mullen RJ, (1978) The development and degeneration of Purkinje cells in pcd mutant mice. J Comp Neurol 177: 125-143.
70. Nolan BC, Freeman JH, (2006) Purkinje cell loss by OX7-saporin impairs acquisition and extinction of eyeblink conditioning. Learn Mem 13: 359-365.
71. Woodruff-Pak DS, Cronholm JF, Sheffield JB, (1990) Purkinje cell number related to rate of classical conditioning. Neuroreport 1: 165-168.
72. Bracha V, Zhao L, Wunderlich DA, Morrissy SJ, Bloedel JR, (1997) Patients with cerebellar lesions cannot acquire but are able to retain conditioned eyeblink reflexes. Brain 20: 1401-1413.
73. Daum I, Channon S, Canavan AG, (1989) Classical conditioning in patients with severe memory problems. J Neurol Neurosurg Psychiatry 52: 47-51.
74. Dimitrova A, Gerwig M, Brol B, Gizewski ER, Forsting M, et al. (2008) Correlation of cerebellar volume with eyeblink conditioning in healthy subjects and in patients with cerebellar cortical degeneration. Brain Res 1198: 73-84.
75. Gerwig M, Kolb FP, Timmann D, (2007) The involvement of the human cerebellum in eyeblink conditioning. Cerebellum 6: 38-57.
76. Topka H, Valls-Sole J, Massaquoi SG, Hallett M, (1993) Deficit in classical conditioning in patients with cerebellar degeneration. Brain 116: 961-969.
77. Chen C, Kano M, Abeliovich A, Chen L, Bao S, et al. (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKCγ mutant mice. Cell 83: 1233-1242.
78. Miyata M, Kishimoto Y, Tanaka M, Hashimoto K, Hirashima N, et al. (2011) A role for myosin Va in cerebellar plasticity and motor learning: a possible mechanism underlying neurological disorder in myosin Va disease. J Neurosci 31: 6067-6078.
79. Rangel A, Madroñal N, Gruart A, Gavín R, Llorens F, et al. (2009) Regulation of GABA(A) and glutamate receptor expression, synaptic facilitation and long-term potentiation in the hippocampus of prion mutant mice. PLoS One 4: e7592.
80. Berger TW, Alger B, Thompson RF, (1976) Neuronal substrate of classical conditioning in the hippocampus. Science 192: 483-485.
81. Gruart A, Muñoz MD, Delgado-García JM, (2006) Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 26: 1077-1087.
82. Solomon PR, Solomon SD, Schaaf EV, Perry HE, (1983) Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 220: 329-331.
83. Woodruff-Pak DS, Li YT, Hinchliffe RM, Port RL, (1997) Hippocampus in delay eyeblink classical conditioning: essential for nefiracetam amelioration of learning in older rabbits. Brain Res 747: 207-218.
84. Kishimoto Y, Kawahara S, Kirino Y, Kadotani H, Nakamura Y, et al. (1997) Conditioned eyeblink response is impaired in mutant mice lacking NMDA receptor subunit NR2A. Neuroreport 8: 3717-3721.
85. Kishimoto Y, Kawahara S, Mori H, Mishina M, Kirino Y, (2001) Long-trace interval eyeblink conditioning is impaired in mutant mice lacking the NMDA receptor subunit ε1. Eur J of Neurosci 13: 1221-1227.
86. Van Der Giessen RS, Koekkoek SK, van Dorp S, De GruijlJR, Cupido A, et al. (2008) Role of olivary electrical coupling in cerebellar motor learning. Neuron 58: 599-612.
87. Bullock D, Fiala JC, Grossberg S, (1994) A neural model of timed response learning in the cerebellum. Neural Netw 7: 1101-1114.
88. Mauk MD, Donegan NH, (1997) A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn Mem 4: 130-158.
89. Bao S, Chen L, Qiao X, Knusel B, Thompson RF, (1998) Impaired eye-blink conditioning in waggler, a mutant mouse with cerebellar BDNF deficiency. Learn Mem 5: 355-364.
90. Qiao X, Chen L, Gao H, Bao S, Hefti F, et al. (1998) Cerebellar brain-derived neurotrophic factor-TrkB defect associated with impairment of eyeblink conditioning in Stargazer mutant mice. J Neurosci 18: 6990-6999.
91. Chen L, Bao S, Qiao X, Thompson RF, (1999) Impaired cerebellar synapse maturation in waggler, a mutant mouse with a disrupted neuronal calcium channel γ subunit. Proc Natl Acad Sci USA 96: 12132-12137.
92. Hashimoto K, Fukaya M, Qiao X, Sakimura K, Watanabe M, et al. (1999) Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J Neurosci 19: 6027-6036.
93. Herms JW, Korte S, Gall S, Schneider I, Dunker S, et al. (2000) Altered intracellular calcium homeostasis in cerebellar granule cells of prion protein-deficient mice. J Neurochem 75: 1487-1492.
94. Herms J, Tings T, Gall S, Madlung A, Giese A, et al. (1999) Evidence of presynaptic location and function of the prion protein. J Neurosci 19: 8866-8875.
95. Prestori F, Rossi P, Bearzatto B, Laine J, Necchi D, et al. (2008) Altered neuron excitability and synaptic plasticity in the cerebellar granular layer of juvenile prion protein knock-out mice with impaired motor control. J Neurosci 28: 7091-7103.
96. Porras-García E, Cendelin J, Domínguez-del-Toro E, Vožeh F, Delgado-García JM, (2005) Purkinje cell loss affects differentially the execution, acquisition and prepulse inhibition of skeletal and facial motor responses in Lurcher mice. Eur J Neurosci 21: 979-988.